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This is the sixth story in a series of articles on frugivory and seed dispersal, leading up to the FSD 2020 symposium in March next year.

Fruits come in a tremendous variety of shapes, sizes, colours, textures, and aromas. What brings this about? One common explanation is that these and other fruit traits have evolved in response to the preferences of animal seed dispersers. Fleshy fruits have evolved to attract animals to feed on the flesh, swallow the seeds, and disperse them. But these animals are all different: a small bird and an elephant might prefer fruits of different sizes; a day-active bird may prefer fruits that look different than those preferred by a night-active primate; a bat may prefer fruits that are accessible to a flying animal, something a tree-climbing animal would care little about. So goes the theory, fruits cannot be appealing to all animals, and have evolved a set of traits that are attractive to only a handful of animal seed dispersers.

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A group of Red-bellied Lemurs (Eulemur rubriventer) pictured in Ranomafana National Park, Madagascar. The lemurs are red-green colourblind but have an excellent sense of smell, which they use for food acquisition and communication with each other. Photograph: N Rowe and Centre ValBio

In this context, the study in focus addressed the question of whether fruit scent – the pleasant and aromatic bouquet of chemicals emitted from ripe fruits – has evolved to allow animals to identify ripe fruits. We analysed the scents of ripe and unripe fruits of plant species growing in the montane rainforest of Ranomafana National Park in eastern Madagascar. First, we looked at fruits that rely on seed dispersal by lemurs. 

Lemurs are a group of primates endemic to Madagascar, which tend to have rather poor colour vision capacities and are sometimes night-active, but have an excellent sense of smell. In other words, if fruits have evolved to communicate with animals through scent, it will be when communicating with lemurs. We found that these fruits tend to significantly change their scent when they become ripe – they increase the amount, but also recruit very different chemical compounds. This means that it is easy to tell if a fruit is ripe based only on how it smells.

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Called ‘Voara’ by the people around Ranomafana National Park, these figs (Ficus tiliifolia) are the perfect example of fruits that have evolved to signal their ripeness through scent. While they barely change their colour when ripe, these figs emit a strong and aromatic scent which informs lemurs that they are ripe. Photograph: Omer Nevo

But these results are not surprising to anyone who has ever seen or smelled ripe and unripe fruits. How can we argue that this is not a pleasant byproduct of fruit maturation or a trait that is present in all fruits? To answer this, we moved on to conduct an identical analysis of fruits that specialise in seed dispersal by birds. Our motivation was that birds tend to have excellent colour vision, but rely less on their sense of smell. We found that in these fruits, unripe fruits smell more or less the same like ripe fruits. This indicates that the aromatic explosion in lemur-dispersed fruits is not just a trivial byproduct of fruit maturation. Rather, it is unique to species that benefit from sending out chemical signals, because their main seed disperser has a keen sense of smell.

A female Red-bellied Lemur (Eulemur rubriventer) feeding on fruits in Ranomafana National Park, Madagascar. The lemurs tend to sniff fruits to decide whether to ingest them or not. Video from Nevo et al. 2018, Science Advances (CC BY-NC).

Finally, we conducted systematic behavioural observations of the Red-bellied Lemur, one of the most common fruit-eating lemurs in eastern Madagascar. We found that when lemurs feed on fruits that tend to change their scent more, they do become more reliant on their sense of smell. This indicates that the lemurs use scent to identify whether a fruit is ripe or not, and that fruit scents do perform the role of a communication channel between plants and animals.

Taken together, these results indicate that the pleasant aroma of fruits is not a trivial byproduct of their ripeness, but a complex communication system which has evolved to help plants and animals communicate.

Original article:

Nevo, O., Razafimandimby, D., Jeffrey, J. A. J., Schulz, S., & Ayasse, M. (2018). Fruit scent as an evolved signal to primate seed dispersal. Science Advances, 4, eaat4871.